Modeling the Oxygen Evolving Complex of Photosystem II
Olbelina A. Ulloa
“Literature Seminar”
09/20/2011
Photosystems are chlorophyll-containing units of proteins that use light to conduct
chemical reactions. Photosystmes in the thylakoid membrane of plants and algae can
produce oxygen for respiration, adenosine triphosphine (ATP) for energy, and
hydrocarbons for food.1,2 Photosystem II (PS II) is the only protein system in nature that
performs the oxidation of water to produce molecular oxygen, protons, and electrons (eq
1).3 The oxygen produced is given off by plants and algae and is used by other organism
in mitochondrial respiration.1 Protons are released into the thylakoid membrane, and
create the gradient that drives ATP synthesis by ATPase. Finally, the electrons produced
are transferred to Photosystem I, where NADPH is produced and used to synthesize
hydrocarbons from carbon dioxide.1
The oxidation of water by PS II occurs at an active site known as the oxygen evolving
complex (OEC). Recently Umena et. al. reported the crystal structure of the 350KDa
system with a 1.9Å resolution. Revealing the previously elusive OEC structure
consisting of a Mn4CaO5 cluster (figure 1). The cluster is an asymmetric Mn3Ca cubane
with an additional dangling Mn, five bridging oxygen, and four terminal water
molecules4,5. The mechanism of water oxidation by the OEC is still greatly debated;4
however it is known to be initiated by four consecutive oxidations of the cluster.1,4,5 It is
suggested that this high oxidation state may form a Mn oxo intermediate with an
electrophilic oxygen, which is susceptible to nucleophilic attack by a second water
molecule3. This O-O bond-forming step is followed by release of molecular oxygen and
regeneration of the low oxidation state cluster. 2,4 The OEC is able to produce oxygen
with turnover numbers of 180,000 molecules of O2 cite-1.
Figure 1. Structure of the oxygen evolving complex.4,5
The OEC is seen as a potential template for the anode of an electrochemical cell
that uses water to produce protons and electrons2. At a cathode these products could be
transformed into molecular hydrogen and be used as fuel.2 This motivation has lead to the
synthesis of many structural and functional models of the OEC 6 Some of the traits
researchers aim to model are, the ability to absorb light and convert it into chemical
potential, the use of chemical oxidants to oxidize water, the structural capability of
storing two to four oxidizing equivalents, and the ability to form a reactive Mn oxo
intermediates to aid in O-O bond formation3,7. In this presentation, two exemplary
models have been chosen to explore some of the traits mentioned above.
Dismukes and coworkers developed the first featured catalyst, a [Mn4O4L6]+
cubium (figure 2) which is capable of electro-oxidizing water at 1.00V (vs. Ag/AgCl)
when illiminated by UV-visible light8. The catalyst is suspended in a proton-conducting
membrane called a nafion that is coated onto a conductive electrode8 The proposed
mechanism proceeds by dissociation of a ligand, and release of O2 to form a “butterfly”
intermediate. The intermediate is able to oxidize two water molecules, and regenarates
the cubium by association of a ligand.8 Catalytic turnover frequencies of up to 270
molecules of O2 hr-1 catalyst-1 and >1000 molecules O2 catalyst-1 have been observed for
this catalyst under mild conditions.9 To overcome the need for applied potential
Dismukes and coworkers designed a molecular based photoelectrochemical cell that
employs nafion-cubium system. A TiO2-supported Ru(bpy)32+ (bpy: 2,2’-bipyridine)
photosensitizers (figure 2) is used to extract electrons from the catalyst providing the
potential to oxidize water without the need of an external voltage. This
photoelectrochemical cell can produce O2 with turnover frequencies of 47 ± 10 O2
molecules hr-1catalyst-1 under mild conditions. 9
Figure 2. [Mn4O4L6]+ cubium as a functional and structural model of the OEC (left).
Ru(bpy)32+ photosenzitizer (right).
Another model for the OEC, Mn2(μ-O)2(terpy)2(H2O)2 3+ (terpy: 2,2';6',2"terpyridine) (figure 3), is a dinuclear Mn complex synthesized by Limburg and
coworkers It is shown to form a Mn oxo intermediate, and catalytically produce O2 with
the help of chemical oxidants.7 The proposed mechanism begins with the oxidation of a
MnIIIMnIV(μ-O)2(terpy)2(H2O)2 3+ by a chemical oxidant. This is followed by formation
of a Mn oxo intermediate, and nucleophilic attack by a second water molecule to form an
O-O bond7. Elimination of O2 and oxidation regenerates the MnIIIMnIV(μO)2(terpy)2(H2O)2 3+ species. The origin of the oxygen in this catalytic system has been
questioned due to the possible oxidation of water by some oxygen-containing chemical
oxidants3 Kinetic experiments demonstrated a first order dependence on the oxidants,
which cannot account for the mechanism where the oxidant is the only source of oxygen.7
Complementary 18O labeling7 and electrochemical studies10 with oxone suggest that water
is in fact a source of one oxygen, but a chemical oxidant is required to produce O2. The
similarities between the OEC and this catalyst make it an important model for the study
of high oxidation intermediates.
Figure 3. Dimeric model [Mn2(O)2(terpy)2(H2O)2 3+] related to the OEC
Models of the OEC have targeted oxidations states, structure, and formation of
proposed intermediates.3 Recent findings by Umena and coworkers on the structure of the
OEC will likely inspire additional work on models.4,5 The importance of other cofactor
such as Ca2+, Cl-, and the hydrogen-bonding network of the system are becoming more
clearly understood, which may also prove beneficial to future biomimetic structures.5
References
(1)
Bertini, I. G., H. B.; Stiefel, E. I.; Valentine, J. S. Biological Inorganic
Chemistry: Structure and Reactivity; University Science Books, 2007.
(2)
Lubitz, W.; Reijerse, E. J.; Messinger, J. Energy Environ. Sci. 2008, 1, 15.
(3)
Herrero, C.; Quaranta, A.; Leibl, W.; Rutherford, A. W.; Aukauloo, A. Energy
Environ. Sci. 2011, 4, 2353.
(4)
Najafpour, M. M.; Govindjee Dalton Trans. 2011, 40, 9076.
(5)
Umena, Y.; Kawakami, K.; Shen, J.-R.; Kamiya, N. Nature 2011, 473, 55.
(6)
Kanady, J. S.; Tsui, E. Y.; Day, M. W.; Agapie, T. Science 2011, 333, 733.
(7)
Limburg, J.; Vrettos, J. S.; Chen, H.; de Paula, J. C.; Crabtree, R. H.; Brudvig, G.
W. J. Am. Chem. Soc. 2001, 123, 423.
(8)
Brimblecombe, R.; Kolling, D. R. J.; Bond, A. M.; Dismukes, G. C.; Swiegers, G.
F.; Spiccia, L. Inorg. Chem. 2009, 48, 7269.
(9)
Brimblecombe, R.; Koo, A.; Dismukes, G. C.; Swiegers, G. F.; Spiccia, L. J. Am.
Chem. Soc. 2010, 132, 2892.
(10)
Baffert, C.; Romain, S.; Richardot, A.; Lepretre, J.-C.; Lefebvre, B.; Deronzier,
A.; Collomb, M.-N. J. Am. Chem. Soc. 2005, 127, 13694.